Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. K E Y W O R D Schromosomal inversion, ecological adaptation, Gadus morhua, gene flow, population divergence ----------------------------------------------------------------------------------------------------------------------------------------------------------------------This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. | INTRODUCTIONLocal adaptation characterizes populations that experience higher inherited fitness in their native habitat compared to members of other populations transferred to the same environment (Kawecki & Ebert, 2004). The degree of such ecological adaptation depends on the directional selection of advantageous traits and is counteracted by high connectivity and resulting homogenizing gene flow, implicating a limited potential for local adaptation in populations experiencing high gene flow (Dobzhansky, 1937;Mayr, 1942;Wright, 1931).Although environmental adaptation can also involve gene expression-induced plastic responses such as morphological, physiological or behavioural changes, these occur without genotypic changes (Reusch, 2014;Via et al., 1995).Most marine fish populations have traditionally been regar...

Accurate prediction of species distribution shifts in the face of climate change requires a sound understanding of population diversity and local adaptations. Previous modeling has suggested that global warming will lead to increased abundance of Atlantic cod (Gadus morhua) in the ocean around Greenland, but the dynamics of earlier abundance fluctuations are not well understood. We applied a retrospective spatiotemporal population genomics approach to examine the temporal stability of cod population structure in this region and to search for signatures of divergent selection over a 78-year period spanning major demographic changes. Analyzing >900 gene-associated single nucleotide polymorphisms in 847 individuals, we identified four genetically distinct groups that exhibited varying spatial distributions with considerable overlap and mixture. The genetic composition had remained stable over decades at some spawning grounds, whereas complete population replacement was evident at others. Observations of elevated differentiation in certain genomic regions are consistent with adaptive divergence between the groups, indicating that they may respond differently to environmental variation. Significantly increased temporal changes at a subset of loci also suggest that adaptation may be ongoing. These findings illustrate the power of spatiotemporal population genomics for revealing biocomplexity in both space and time and for informing future fisheries management and conservation efforts.